Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T06:51:48.399Z Has data issue: false hasContentIssue false

Olfactory hallucinations in Alzheimer’s disease

Published online by Cambridge University Press:  28 September 2020

Mohamad El Haj*
Affiliation:
Nantes Université, Univ Angers, Laboratoire de Psychologie des Pays de la Loire (LPPL – EA 4638), F-44000Nantes, France Unité de Gériatrie, Centre Hospitalier de Tourcoing, Tourcoing, France Institut Universitaire de France, Paris, France
Frank Larøi
Affiliation:
Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway Norwegian Center of Excellence for Mental Disorders Research, University of Oslo, Oslo, Norway Psychology and Neuroscience of Cognition Research Unit, University of Liège, Liège, Belgium
*
Author for correspondence: Mohamad El Haj, Email: [email protected]

Abstract

We assessed the frequency, duration, and degree of unpleasantness of olfactory hallucinations in Alzheimer’s disease (AD). Informants of 31 AD patients were invited to rate the frequency, duration, and degree of unpleasantness of olfactory, auditory, and visual hallucinations. Analysis demonstrated little occurrence of olfactory hallucinations compared with auditory or visual hallucinations. Results also demonstrated that olfactory hallucinations span from a few seconds to one minute, a duration that was similar to that of auditory and visual hallucinations. Olfactory hallucinations were rated as unpleasant compared with auditory or visual hallucinations. Finally, olfactory hallucinations were significantly correlated with depression. Our findings demonstrate little occurrence of olfactory hallucinations but that when they occur, they are experienced as relatively unpleasant in AD patients. Our findings also demonstrate a relationship between olfactory hallucinations and psychiatric characteristics (i.e., depression) in AD.

Type
Original Article
Copyright
© Scandinavian College of Neuropsychopharmacology 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Badcock, JC, Waters, FA and Maybery, M (2007) On keeping (intrusive) thoughts to one’s self: testing a cognitive model of auditory hallucinations. Cognitive Neuropsychiatry 12, 7889.CrossRefGoogle ScholarPubMed
Ballard, C, Holmes, C, Mckeith, I, Neill, D, O’Brien, J, Cairns, N, Lantos, P, Perry, E, Ince, P and Perry, R (1999) Psychiatric morbidity in dementia with Lewy bodies: a prospective clinical and neuropathological comparative study with Alzheimer’s disease. The American Journal of Psychiatry 156, 10391045.Google ScholarPubMed
Bassiony, MM and Lyketsos, CG (2003) Delusions and hallucinations in Alzheimer’s disease: review of the brain decade. Psychosomatics 44, 388401.CrossRefGoogle ScholarPubMed
Basso, M, Yang, J, Warren, L, Macavoy, MG, Varma, P, Bronen, RA and Van Dyck, CH (2006) Volumetry of amygdala and hippocampus and memory performance in Alzheimer’s disease. Psychiatry Research 146, 251261.CrossRefGoogle ScholarPubMed
Birchwood, M and Chadwick, P (1997) The omnipotence of voices: testing the validity of a cognitive model. Psychological Medicine 27, 13451353.CrossRefGoogle ScholarPubMed
Campbell, S, Marriott, M, Nahmias, C and Macqueen, GM (2004) Lower hippocampal volume in patients suffering from depression: a meta-analysis. The American Journal of Psychiatry 161, 598607.CrossRefGoogle ScholarPubMed
Chaudhury, S (2010) Hallucinations: clinical aspects and management. Indian Journal of Psychiatry 19, 512.CrossRefGoogle ScholarPubMed
Cohen, J (1992) Statistical power analysis. Current Directions in Psychological Science 1, 98101.CrossRefGoogle Scholar
Deems, DA, Doty, RL, Settle, RG, Moore-Gillon, V, Shaman, P, Mester, AF, Kimmelman, CP, Brightman, VJ and Snow, JB (1991) Smell and taste disorders, a study of 750 patients from the University of Pennsylvania Smell and Taste Center. Archives of Otolaryngology - Head and Neck Surgery 117, 519528.CrossRefGoogle ScholarPubMed
Diniz, BS, Butters, MA, Albert, SM, Dew, MA and Reynolds, CF 3rd (2013) Late-life depression and risk of vascular dementia and Alzheimer’s disease: systematic review and meta-analysis of community-based cohort studies. British Journal of Psychiatry 202, 329335.CrossRefGoogle ScholarPubMed
El Haj, M (2016) Memory suppression in Alzheimer’s disease. Neurological sciences 37, 337343.CrossRefGoogle ScholarPubMed
El Haj, M, Antoine, P, Amouyel, P, Lambert, JC, Pasquier, F and Kapogiannis, D (2016a) Apolipoprotein E (APOE) epsilon4 and episodic memory decline in Alzheimer’s disease: a review. Ageing Research Reviews 27, 1522.CrossRefGoogle ScholarPubMed
El Haj, M, Antoine, P, Nandrino, JL and Kapogiannis, D (2015a) Autobiographical memory decline in Alzheimer’s disease, a theoretical and clinical overview. Ageing Research Reviews 23, 183192.CrossRefGoogle ScholarPubMed
El Haj, M, Jardri, R, Laroi, F and Antoine, P (2016b) Hallucinations, loneliness, and social isolation in Alzheimer’s disease. Cognitive Neuropsychiatry 21, 113.CrossRefGoogle ScholarPubMed
El Haj, M, Laroi, F, Gely-Nargeot, MC and Raffard, S (2015b) Inhibitory deterioration may contribute to hallucinations in Alzheimer’s disease. Cognitive Neuropsychiatry 20, 281295.CrossRefGoogle ScholarPubMed
El Haj, M, Roche, J, Jardri, R, Kapogiannis, D, Gallouj, K and Antoine, P (2017) Clinical and neurocognitive aspects of hallucinations in Alzheimer’s disease. Neuroscience & Biobehavioral Reviews 83, 713720.CrossRefGoogle ScholarPubMed
Ellis, PD (2010) The Essential Guide to Effect Sizes: Statistical Power, Meta-Analysis, and the Interpretation of Research Results. New York, NY: Cambridge University Press.CrossRefGoogle Scholar
Faulcon, P, Portier, F, Biacabe, B and Bonfils, P (1999) Anosmia secondary to acute rhinitis: clinical signs and course in a series of 118 patients. Annales Françaises d’Oto-Rhino-Laryngologie Cervicofac 116, 351357.Google Scholar
Folstein, MF, Folstein, SE and Mchugh, PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189198.CrossRefGoogle ScholarPubMed
Graves, AB, Bowen, JD, Rajaram, L, Mccormick, WC, Mccurry, SM, Schellenberg, GD and Larson, EB (1999) Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E ϵ4 status. Neurology 53, 1480.CrossRefGoogle Scholar
Grober, E and Buschke, H (1987) Genuine memory deficits in dementia. Developmental Neuropsychology 3, 1336.CrossRefGoogle Scholar
Hamilton, JP, Siemer, M and Gotlib, IH (2008) Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Molecular Psychiatry 13, 9931000.CrossRefGoogle ScholarPubMed
Handley, OJ, Morrison, CM, Miles, C and Bayer, AJ (2006) ApoE gene and familial risk of Alzheimer’s disease as predictors of odour identification in older adults. Neurobiology of Aging 27, 14251430.CrossRefGoogle ScholarPubMed
Hemsley, DR (2005) The development of a cognitive model of schizophrenia: placing it in context. Neuroscience & Biobehavioral Reviews 29, 977988.CrossRefGoogle ScholarPubMed
Jeste, DV and Finkel, SI (2000) Psychosis of Alzheimer’s disease and related dementias. Diagnostic criteria for a distinct syndrome. The American Journal of Geriatric Psychiatry 8, 2934.CrossRefGoogle ScholarPubMed
Jost, BC and Grossberg, GT (1996) The evolution of psychiatric symptoms in Alzheimer’s disease: a natural history study. Journal of the American Geriatrics Society 44, 10781081.CrossRefGoogle ScholarPubMed
Kesner, RP, Gilbert, PE and Barua, LA (2002) The role of the hippocampus in memory for the temporal order of a sequence of odors. Behavioral Neuroscience 116, 286290.CrossRefGoogle ScholarPubMed
Kopala, LC, Good, KP and Honer, WG (1994) Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophrenia Research 12, 205211.CrossRefGoogle ScholarPubMed
Lyketsos, CG, Sheppard, J-ME, Steinberg, M, Tschanz, JAT, Norton, MC, Steffens, DC and Breitner, JCS (2001) Neuropsychiatric disturbance in Alzheimer’s disease clusters into three groups: the Cache County study. International Journal of Geriatric Psychiatry 16, 10431053.CrossRefGoogle ScholarPubMed
Marine, N and Boriana, A (2014) Olfactory markers of depression and Alzheimer’s disease. Neuroscience & Biobehavioral Reviews 45, 262270.Google ScholarPubMed
Mckhann, GM, Knopman, DS, Chertkow, H, Hyman, BT, JackKawas, CRCH JrKawas, CH, Klunk, WE, Koroshetz, WJ, Manly, JJ, Mayeux, R, Mohs, RC, Morris, JC, Rossor, MN, Scheltens, P, Carrillo, MC, Thies, B, Weintraub, S and Phelps, CH (2011) The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia 7, 263269.CrossRefGoogle Scholar
Mega, MS, Lee, L, Dinov, ID, Mishkin, F, Toga, AW and Cummings, JL (2000) Cerebral correlates of psychotic symptoms in Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry 69, 167171.CrossRefGoogle ScholarPubMed
Negoias, S, Croy, I, Gerber, J, Puschmann, S, Petrowski, K, Joraschky, P and Hummel, T (2010) Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience 169, 415421.CrossRefGoogle ScholarPubMed
Poulin, SP, Dautoff, R, Morris, JC, Barrett, LF, Dickerson, BC and Alzheimer’s Disease Neuroimaging Initiative (2011) Amygdala atrophy is prominent in early Alzheimer’s disease and relates to symptom severity. Psychiatry Research 194, 713.CrossRefGoogle ScholarPubMed
Pouliot, S and Jones-Gotman, M (2008) Medial temporal-lobe damage and memory for emotionally arousing odors. Neuropsychologia 46, 11241134.CrossRefGoogle ScholarPubMed
Rosenthal, R and Dimatteo, MR (2001) Meta-analysis: recent developments in quantitative methods for literature reviews. Annual Review of Psychology 52, 5982.CrossRefGoogle ScholarPubMed
Rubin, EH, Drevets, WC and Burke, WJ (1988) The nature of psychotic symptoms in senile dementia of the Alzheimer type. Journal of Geriatric Psychiatry and Neurology 1, 1620.Google ScholarPubMed
Rubinow, MJ, Mahajan, G, May, W, Overholser, JC, Jurjus, GJ, Dieter, L, Herbst, N, Steffens, DC, Miguel-Hidalgo, JJ, Rajkowska, G and Stockmeier, CA (2016) Basolateral amygdala volume and cell numbers in major depressive disorder: a postmortem stereological study. Brain Structure and Function 221, 171184.CrossRefGoogle ScholarPubMed
Scarmeas, N, Brandt, J, Albert, M, Hadjigeorgiou, G, Papadimitriou, A, Dubois, B, Sarazin, M, Devanand, D, Honig, L, Marder, K, Bell, K, Wegesin, D, Blacker, D and Stern, Y (2005) Delusions and hallucinations are associated with worse outcome in Alzheimer disease. Archives of Neurology 62, 16011608.CrossRefGoogle ScholarPubMed
Seo, HS, Jeon, KJ, Hummel, T and Min, BC (2009) Influences of olfactory impairment on depression, cognitive performance, and quality of life in Korean elderly. European Archives of Oto-Rhino-Laryngology 266, 17391745.CrossRefGoogle ScholarPubMed
Soriano, MF, Jimenez, JF, Roman, P and Bajo, MT (2009) Intentional inhibition in memory and hallucinations: directed forgetting and updating. Neuropsychology 23, 6170.CrossRefGoogle ScholarPubMed
Speck, CE, Kukull, WA, Brenner, DE, Bowen, JD, Mccormick, WC, Ten, L, Pfanschmidt, ML, Thompson, JD and Larson, EB (1995) History of depression as a risk factor for Alzheimer’s disease. Epidemiology 6, 366369.CrossRefGoogle ScholarPubMed
Steinberg, M, Sheppard, JM, Tschanz, JT, Norton, MC, Steffens, DC, Breitner, JC and Lyketsos, CG (2003) The incidence of mental and behavioral disturbances in dementia: the cache county study. The Journal of Neuropsychiatry and Clinical Neurosciences 15, 340345.CrossRefGoogle ScholarPubMed
Stevenson, RJ, Langdon, R and Mcguire, J (2011) Olfactory hallucinations in schizophrenia and schizoaffective disorder: a phenomenological survey. Psychiatry Research 185, 321327.CrossRefGoogle ScholarPubMed
Tariot, PN, Mack, JL, Patterson, MB, Edland, SD, Weiner, MF, Fillenbaum, G, Blazina, L, Teri, L, Rubin, E, Mortimer, JA and Stern, Y (1995) The Behavior Rating Scale for Dementia of the Consortium to Establish a Registry for Alzheimer’s Disease. The Behavioral Pathology Committee of the Consortium to Establish a Registry for Alzheimer’s Disease. The American Journal of Psychiatry 152, 13491357.Google Scholar
Thomann, PA, Dos Santos, V, Toro, P, Schonknecht, P, Essig, M and Schroder, J (2009) Reduced olfactory bulb and tract volume in early Alzheimer’s disease--a MRI study. Neurobiology of Aging 30, 838841.CrossRefGoogle ScholarPubMed
Tsuang, D, Larson, EB, Bolen, E, Thompson, ML, Peskind, E, Bowen, J, Mccormick, W, Teri, L, Kukull, W, Vavrek, D, Montine, T and Leverenz, JB (2009) Visual hallucinations in dementia: a prospective community-based study with autopsy. The American Journal of Geriatric Psychiatry 17, 317323.CrossRefGoogle ScholarPubMed
Waters, FA, Badcock, JC, Maybery, MT and Michie, PT (2003) Inhibition in schizophrenia: association with auditory hallucinations. Schizophrenia Research 62, 275280.CrossRefGoogle ScholarPubMed
Wilson, RS, Gilley, DW, Bennett, DA, Beckett, LA and Evans, DA (2000) Hallucinations, delusions, and cognitive decline in Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry 69, 172177.CrossRefGoogle ScholarPubMed
Wilson, RS, Krueger, KR, Kamenetsky, JM, Tang, Y, Gilley, DW, Bennett, DA and Evans, DA (2005) Hallucinations and mortality in Alzheimer disease. The American Journal of Geriatric Psychiatry 13, 984990.CrossRefGoogle ScholarPubMed
Zigmond, AS and Snaith, RP (1983) The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica 67, 361370.CrossRefGoogle ScholarPubMed